Delineating gray and white matter involvement in brain lesions: three-dimensional alignment of functional magnetic resonance imaging and diffusion-tensor imaging

Talma Hendler M.D., Ph.D. 1 , Pazit Pianka M.D. 1 , Michal Sigal B.Sc. 1 , Michal Kafri M.Sc. 1 , Dafna Ben-Bashat Ph.D. 1 , Shlomi Constantini M.D., M.Sc. 1 , Moshe Graif M.D. 1 , Itzhak Fried M.D., Ph.D. 1 and Yaniv Assaf Ph.D. 1
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  • 1 Functional Brain Imaging Unit, Wohl Institute for Advanced Imaging; Functional Neurosurgery Unit, Tel-Aviv Sourasky Medical Center; Faculty of Medicine; School of Chemistry, Tel-Aviv University; Department of Pediatric Neurosurgery, Dana Children's Hospital, Tel-Aviv, Israel; Division of Neurosurgery, Center for Health Sciences, University of California at Los Angeles, California; and Laboratory of Brain and Cognition, National Institutes of Mental Health, National Institutes of Health, Bethesda, Maryland

Object. The role of functional magnetic resonance (fMR) imaging has become increasingly important in the presurgical mapping of gray matter. Neurosurgical interventions often involve fiber bundles that connect critical functional areas. Recently, diffusion-tensor (DT) imaging has enabled the visualization of fiber bundle direction and integrity, thus providing the ability to delineate clearly white matter from gray matter tissue. The main objective of this study was to improve the presurgical assessment of critical functionality in the vicinity of brain lesions by combining DT and fMR imaging methodologies.

Methods. Twenty patients with various space-occupying brain lesions underwent imaging for presurgical evaluation of motor and/or somatosensory functions. The authors focus on five patients with diverse space-occupying brain lesions. Diffusion tensor—based fiber tracking and fMR imaging activation maps were superimposed in three dimensions to visualize pyramidal tracts corresponding to motor and somatosensory regional activation.

Conclusions. The combination of DT and fMR imaging for presurgical functional brain mapping provides valuable information that cannot be extracted using either method alone. The validity and sensitivity of noninvasive functional mapping for surgical guidance could be improved by considering results obtained with both methods. Furthermore, the use of three-dimensional visualization seems crucial and unique for viewing and understanding the complicated spatial relationship among the lesion, gray matter activation, and white matter fiber bundles.

Contributor Notes

Address reprint requests to: Yaniv Assaf, Ph.D., Department of Radiology, Functional Brain Imaging Unit, The Wohl Institute for Advanced Imaging, Tel-Aviv Sourasky Medical Center, 6 Weizman Street, Tel-Aviv 64239, Israel. email: assafyan@post.tau.ac.il.
  • 1.

    Arthurs OJ, & Boniface S: How well do we understand the neural origins of the fMRI BOLD signal? Trends Neurosci 25:2731, 2002 Arthurs OJ, Boniface S: How well do we understand the neural origins of the fMRI BOLD signal? Trends Neurosci 25:27–31, 2002

    • Search Google Scholar
    • Export Citation
  • 2.

    Assaf Y, , Ben-Bashat D, & Chapman J, et al: High b-value q-space analyzed diffusion-weighted MRI: application to multiple sclerosis. Magn Reson Med 47:115126, 2002 Assaf Y, Ben-Bashat D, Chapman J, et al: High b-value q-space analyzed diffusion-weighted MRI: application to multiple sclerosis. Magn Reson Med 47:115–126, 2002

    • Search Google Scholar
    • Export Citation
  • 3.

    Basser PJ, , Mattiello J, & Le-Bihan D: MR diffusion tensor spectroscopy and imaging. Biophys J 66:259267, 1994 Basser PJ, Mattiello J, Le-Bihan D: MR diffusion tensor spectroscopy and imaging. Biophys J 66:259–267, 1994

    • Search Google Scholar
    • Export Citation
  • 4.

    Basser PJ, , Pajevic S, & Pierpaoli C, et al: In vivo fiber tractography using DT-MRI data. Magn Reson Med 44:625632, 2000 Basser PJ, Pajevic S, Pierpaoli C, et al: In vivo fiber tractography using DT-MRI data. Magn Reson Med 44:625–632, 2000

    • Search Google Scholar
    • Export Citation
  • 5.

    Basser PJ, & Pierpaoli C: A simplified method to measure the diffusion tensor from seven MR images. Magn Reson Med 39:928934, 1998 Basser PJ, Pierpaoli C: A simplified method to measure the diffusion tensor from seven MR images. Magn Reson Med 39:928–934, 1998

    • Search Google Scholar
    • Export Citation
  • 6.

    Conturo TE, , Lori NF, & Cull TS, et al: Tracking neuronal fiber pathways in the living human brain. Proc Natl Acad Sci USA 96:1042210427, 1999 Conturo TE, Lori NF, Cull TS, et al: Tracking neuronal fiber pathways in the living human brain. Proc Natl Acad Sci USA 96:10422–10427, 1999

    • Search Google Scholar
    • Export Citation
  • 7.

    DeYoe EA, , Bandettini P, & Neitz J, et al: Functional magnetic resonance imaging (FMRI) of the human brain. J Neurosci Methods 54:171187, 1994 DeYoe EA, Bandettini P, Neitz J, et al: Functional magnetic resonance imaging (FMRI) of the human brain. J Neurosci Methods 54:171–187, 1994

    • Search Google Scholar
    • Export Citation
  • 8.

    Heeger DJ, & Ress D: What does fMRI tell us about neuronal activity? Nat Rev Neurosci 3:142151, 2002 Heeger DJ, Ress D: What does fMRI tell us about neuronal activity? Nat Rev Neurosci 3:142–151, 2002

    • Search Google Scholar
    • Export Citation
  • 9.

    Holodny AI, & Ollenschlager M: Diffusion imaging in brain tumors. Neuroimaging Clin N Am 12:107124, 2002 Holodny AI, Ollenschlager M: Diffusion imaging in brain tumors. Neuroimaging Clin N Am 12:107–124, 2002

    • Search Google Scholar
    • Export Citation
  • 10.

    Holodny AI, , Ollenschleger MD, & Liu WC, et al: Identification of the corticospinal tracts achieved using blood-oxygen-level-dependent and diffusion functional MR imaging in patients with brain tumors. AJNR 22:8388, 2001 Holodny AI, Ollenschleger MD, Liu WC, et al: Identification of the corticospinal tracts achieved using blood-oxygen-level-dependent and diffusion functional MR imaging in patients with brain tumors. AJNR 22:83–88, 2001

    • Search Google Scholar
    • Export Citation
  • 11.

    Kraemer F, , Darquie A, & Clark CA, et al: Separation of two diffusion compartments in the human brain. Proc Intl Soc Magn Reson Med 7:1808, 1999 (Abstract) Kraemer F, Darquie A, Clark CA, et al: Separation of two diffusion compartments in the human brain. Proc Intl Soc Magn Reson Med 7:1808, 1999 (Abstract)

    • Search Google Scholar
    • Export Citation
  • 12.

    Logothetis NK, , Pauls J, & Augath M, et al: Neurophysiological investigation of the basis of the fMRI signal. Nature 412:150157, 2001 Logothetis NK, Pauls J, Augath M, et al: Neurophysiological investigation of the basis of the fMRI signal. Nature 412:150–157, 2001

    • Search Google Scholar
    • Export Citation
  • 13.

    Lundquist P, , Backlund EO, & Sjoqvist L, et al: Clinical application of functional magnetic resonance imaging (fMRI) to surgery in the brain. J Neuroimaging 7:131133, 1997 Lundquist P, Backlund EO, Sjoqvist L, et al: Clinical application of functional magnetic resonance imaging (fMRI) to surgery in the brain. J Neuroimaging 7:131–133, 1997

    • Search Google Scholar
    • Export Citation
  • 14.

    Lurito JT, , Lowe MJ, & Sartorius C, et al: Comparison of fMRI and intraoperative direct cortical stimulation in localization of receptive language areas. J Comput Assist Tomogr 24:99105, 2000 Lurito JT, Lowe MJ, Sartorius C, et al: Comparison of fMRI and intraoperative direct cortical stimulation in localization of receptive language areas. J Comput Assist Tomogr 24:99–105, 2000

    • Search Google Scholar
    • Export Citation
  • 15.

    Mori S, , Crain BJ, & Chacko VP, et al: Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45:265269, 1999 Mori S, Crain BJ, Chacko VP, et al: Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45:265–269, 1999

    • Search Google Scholar
    • Export Citation
  • 16.

    Mori S, , Frederiksen K, & van Zijl PC, et al: Brain white matter anatomy of tumor patients evaluated with diffusion tensor imaging. Ann Neurol 51:377380, 2002 Mori S, Frederiksen K, van Zijl PC, et al: Brain white matter anatomy of tumor patients evaluated with diffusion tensor imaging. Ann Neurol 51:377–380, 2002

    • Search Google Scholar
    • Export Citation
  • 17.

    Pajevic S, & Pierpaoli C: Color schemes to represent the orientation of anisotropic tissues from diffusion tensor data: application to white matter fiber tract mapping in the human brain. Magn Reson Med 42:526540, 1999 Pajevic S, Pierpaoli C: Color schemes to represent the orientation of anisotropic tissues from diffusion tensor data: application to white matter fiber tract mapping in the human brain. Magn Reson Med 42:526–540, 1999

    • Search Google Scholar
    • Export Citation
  • 18.

    Price CJ, & Friston KJ: Degeneracy and cognitive anatomy. Trends Cogn Sci 6:416421, 2002 Price CJ, Friston KJ: Degeneracy and cognitive anatomy. Trends Cogn Sci 6:416–421, 2002

    • Search Google Scholar
    • Export Citation
  • 19.

    Roux FE, , Boulanouar K, & Ranjeva JP, et al: Cortical intraoperative stimulation in brain tumors as a tool to evaluate spatial data from motor functional MRI. Invest Radiol 34:225229, 1999 Roux FE, Boulanouar K, Ranjeva JP, et al: Cortical intraoperative stimulation in brain tumors as a tool to evaluate spatial data from motor functional MRI. Invest Radiol 34:225–229, 1999

    • Search Google Scholar
    • Export Citation
  • 20.

    Sinha S, , Bastin ME, & Whittle IR, et al: Diffusion tensor MR imaging of high-grade cerebral gliomas. AJNR 23:520527, 2002 Sinha S, Bastin ME, Whittle IR, et al: Diffusion tensor MR imaging of high-grade cerebral gliomas. AJNR 23:520–527, 2002

    • Search Google Scholar
    • Export Citation
  • 21.

    Talairach J, & Tournoux P: Co-planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging. New York: Thieme Medical Publishers, 1988 Talairach J, Tournoux P: Co-planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging. New York: Thieme Medical Publishers, 1988

    • Search Google Scholar
    • Export Citation
  • 22.

    Tomczak RJ, , Wunderlich AP, & Wang Y, et al: fMRI for preoperative neurosurgical mapping of motor cortex and language in a clinical setting. J Comput Assist Tomogr 24:927934, 2000 Tomczak RJ, Wunderlich AP, Wang Y, et al: fMRI for preoperative neurosurgical mapping of motor cortex and language in a clinical setting. J Comput Assist Tomogr 24:927–934, 2000

    • Search Google Scholar
    • Export Citation
  • 23.

    Turner R: fMRI: methodology—sensorimotor function mapping. Adv Neurol 83:213220, 2000 Turner R: fMRI: methodology—sensorimotor function mapping. Adv Neurol 83:213–220, 2000

    • Search Google Scholar
    • Export Citation
  • 24.

    Werring DJ, , Toosy AT, & Clark CA, et al: Diffusion tensor imaging can detect and quantify corticospinal tract degeneration after stroke. J Neurol Neurosurg Psychiatry 69:269272, 2000 Werring DJ, Toosy AT, Clark CA, et al: Diffusion tensor imaging can detect and quantify corticospinal tract degeneration after stroke. J Neurol Neurosurg Psychiatry 69:269–272, 2000

    • Search Google Scholar
    • Export Citation
  • 25.

    Wieshmann UC, , Krakow K, & Symms MR, et al: Combined functional magnetic resonance imaging and diffusion tensor imaging demonstrate widespread modified organisation in malformation of cortical development. J Neurol Neurosurg Psychiatry 70:521523, 2001 Wieshmann UC, Krakow K, Symms MR, et al: Combined functional magnetic resonance imaging and diffusion tensor imaging demonstrate widespread modified organisation in malformation of cortical development. J Neurol Neurosurg Psychiatry 70:521–523, 2001

    • Search Google Scholar
    • Export Citation
  • 26.

    Wieshmann UC, , Symms MR, & Parker GJ, et al: Diffusion tensor imaging demonstrates deviation of fibres in normal appearing white matter adjacent to a brain tumor. J Neurol Neurosurg Psychiatry 68:501503, 2000 Wieshmann UC, Symms MR, Parker GJ, et al: Diffusion tensor imaging demonstrates deviation of fibres in normal appearing white matter adjacent to a brain tumor. J Neurol Neurosurg Psychiatry 68:501–503, 2000

    • Search Google Scholar
    • Export Citation
  • 27.

    Witwer BP, , Moftakhar R, & Hasan KM, et al: Diffusion-tensor imaging of white matter tracks in patients with cerebral neoplasm. J Neurosurg 97:568575, 2002 Witwer BP, Moftakhar R, Hasan KM, et al: Diffusion-tensor imaging of white matter tracks in patients with cerebral neoplasm. J Neurosurg 97:568–575, 2002

    • Search Google Scholar
    • Export Citation
  • 28.

    Zelaya F, , Flood N, & Chalk JB, et al: An evaluation of the time dependence of the anisotropy of the water diffusion tensor in acute human ischemia. Magn Reson Imaging 17:331348, 1999 Zelaya F, Flood N, Chalk JB, et al: An evaluation of the time dependence of the anisotropy of the water diffusion tensor in acute human ischemia. Magn Reson Imaging 17:331–348, 1999

    • Search Google Scholar
    • Export Citation

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